Reproductive System Structure, Development and Function in Cephalopods with a New General Scale for Maturity Stages pot

http://journal.nafo.int J Northw Atl Fish Sci., Vol 12: 63-74 Reproductive System Structure, Development and Function in Cephalopods with a New General Scale for Maturity Stages A I Arkhipkin Atlantic Research Institute of Marine Fisheries and Oceanography (AtlantNIRO) Dmitry Donskoy Street, Kaliningrad, 236000, USSR Abstract The main types of reproductive system structure, development and functions in cephalopods are described from personal observations and use of the literature There is one type in males and three in females which are order specific These have provided a basis for examining possible evolutionary trends in reproductive system development and in reproductive strategies within coleoid cephalopods and for developing a general scale for maturity staging for males and females Development of the cephalopod reproductive system consists of two main phases The first includes sexual cell differentiation, growth and maturation (i.e juvenile phase and physiological maturation) The second begins after maturation of sexual cells It includestheirtransportand accumulation in different parts of the reproductive system and their conversion into spermatophores in males and eggs with protective coverings in females (i.e physiological maturity, functional maturation and maturity) It was found that species with different life styles within each order have similar reproductive systems This may be attributable to the relative youth in an evolutionary sense of the main groups of living cephalopods A general scale of seven maturity stages for cephalopods was developed Distinct characteristics of each stage are described and supplemented with a generalized drawing of gonad structure In the first phase of reproductive system development, maturity stages are distinguished by the degree of development of the gonad and accessory glands In the second phase maturity stages are distinguished by the fate of the mature sexual cells, particularly by their transport and location in different parts of the reproductive system up to the time of spawning Introduction A structure of the reproductive system in cephalopod males and females usually has been included in descriptions of new species There are several thorough reviews on reproductive system structure forthe main cephalopod orders (Arnold and Williams-Arnold, 1977; Wells and Wells, 1977; Nesis, 1982) Thedevelopment and function of the reproductive system have been studied to a much lesser extent Detailed descriptions are available only for a dozen of the most important commercial species, particularly the Ommastrephidae and Loliginidae such as IIlex illecebrosus (Durward et al., 1979; Burukovsky et al., MS 1984) and Loligo opalescens (Fields, 1965; Grieb and Beeman, 1978) Evolution of the reproductive system in cephalopods as well as cephalopod reproductive strategies have received little attention Reproductive strategies of cephalopods were studied by von Boletzky (1981, 1986) but even in the most recent edition of "Paleontology and Neonatology of Cephalopods" (The Molluscs, 1988) there is no consideration of the evolution of the cephalopod reproductive system Various scales have been developed for cephalopod maturity stage determination (Juanico, 1983) Traditionally authors developed and used their own scales Criteria for dividing the process of sexual development into maturity scale usually involve complex sexual characters Common terminology for cephalopod maturity stages include juvenile, immature, maturing, mature and spent However, authors often apply different meaning to these (Juanico, 1983) and such broadly used terms create difficulties when standard criteria are required for maturity staging Maturity scales with well defined visual, meristic and weight characteristics are available, for instance, for IIlex illecebrosus (Burukovsky et al., MS 1984; Nigmatullin et al., MS 1984) and Sthenoteuthis pteropus (Burukovskyetal., 1977; Zuevetal., 1985) The authors point out that patterns of gonad and accessory gland development are species-specific and it is necessary to develop a maturity scale for each This approach, however, makes comparison of the development of reproductive systems in different species very difficult Therefore it seems worthwhile to develop a general maturity scale for cephalopods which could be used to describe and distinguish all the stages of sexual devel- 64 J Northw Atl Fish Sci., Vol 12, 1992 opment in males and females of different species Such a scale should describe the same processes of reproductive system development by the same maturity stages and should be convenient for the study and comparison of reproductive systems as well as reproductive strategies The purpose of this paper is to describe the main types of reproductive system structure, development and function in all living cephalopod orders of the Subtype Coleoidea This has provided a basis for examining possible evolutionary trends in reproductive system development and in reproductive strategies within coleoid cephalopods and for developing a general scale for maturity staging for males and females Materials and Methods Details of the structure of the reproductive system of the Ommastrephidae squids IIlex illecebrosus (juveniles mainly), Dosidicus gigas and Sthenoteuthis pteropus (from juveniles to adult), IIlex argentinus (adults mainly) were obtained from biological dissections of several thousand specimens Details for other species were obtained from the literature Additionally, V V Laptikhovsky (AtlantNIRO, Kaliningrad, pers comm.) kindly provided results of his studies of oocyte state in ovaries of 50 individuals of 14 species as follows: Octopus vulgaris (3 specimens), Argonauta argo (1 specimen), Tremoctopus violaceus (4 specimens), Sepia bertheloti (3 specimens), Sepiella ornata (1 specimen), Abraliopsis atlantica (8 specimens), Pterigioteuthis gemmata (7 specimens), Onychoteuthis banksi (2 specimens), IIlex argentinus (13 specimens), Todaropsis eblanae (1 specimen), Ornithoteuthis antillarum (1 specimen), Gonatus fabricii (3 specimens), Octopoteuthis sicula (1 specimen), Histioteuthis reversa (2 specimens) He determined dimensions, presence or absence of nucleoli in nuclei, and in most cases, degree of follicle formation A five-level scale of maturity stages for squids used at the AtlantNIRO laboratory (Burukovsky et al., 1977) was the basis for developing a general scale for cephalopod maturity states Characteristics of each stage were described using the terminology of Nigmatullin and Sabirov (1987) and Burukovskyetal (1977) Possible evolution of living cephalopods was considered according to Nesis (1985), characters of r- and k- type reproductive strategies were determined according to Boletzky (1981) Structure of the Reproductive System Cephalopods are short-cyclic and monocyclic (with the exception of Nautilus) animals with a structu- rally complex reproductive system In general, the system in males and females consists of a gonad (testis and ovary) located in the coelom in the posterior part of the body, one or two separate gonoducts and a 'complex of accessory glands which produce different secretion for enhancement and protection of ripe sexual cells The main types of reproductive system structure in cephalopods are illustrated in Fig Females The reproductive system is simplest in the octopus The gonad is oval with two tubular oviducts The oviducal glands are set on the oviducts like a ring and are attached to the sexual coelom (Wells and Wells, 1977) The reproductive system is more complex in cuttlefish than in the octopus The ovary is semi-spherical with two straight oviducts Accessory glands are of three kinds Oviducal glands, in contrast to those of the octopus, are found in the distal end of oviduct positioned in a way such that occytes emerging from the oviducts pass their cavities There are also nidamental glands which are usually oval and accessory nidamental glands whose function is unknown (Nesis, 1982) A diversity of reproductive system structure is found in squid As a rule, the gonad is conical Only one oviduct is developed in some (subfamily Pyroteuthinae and suborder Myopsida) and both are developed in others (the remainder of the suborder Oegopsida) Oviducts are strongly curved tubes with a small funnelshaped entrance Three kinds of accessory glands are present in suborder Myopsida (oviducal, nidarnental and accessory), while in the suborder Oegopsida only oviducal and nidamental glands are found In the subfamily Enoploteuthinae, oviducal glands are well developed but nidamental glands are present Males The structure of the reproductive system is more uniform than in females among the orders of coeloid cephalopods The single testis is rounded (in octopus) or conical (in cuttlefish and squid) The spermduct is usually unpaired and curved with its proximal end enlarged to form an ampulla The spermduct extends into a spermatophoric gland where the spermatophore is formed The spermatophore is characteristic of the male cephalopod The spermatophoric gland is connected by the spermatophoric duct to the Needham sac (spermatophore depository) The distal part of the Needham sac is muscular and functions as a penis In some species the spermatophoric organs are paired, e.g in Histioteuthis hoylei, Selenoteuthis scintillans and Oregonioteuthis springeri (Nesis, 1982) In general, the male reproductive system is more complicated than in females, especially because of the greater number of accessory glands involved in spermatophore formation ARKHIPKIN: Reproductive System Structure, Development and Function in Cephalopods Maturity Stage IV V VI VII I IITI2Th Octopus female I I I I~ Cuttlefish female I~ I I Squid female !:::::: I I ~ : : : : :::!!(::::::~::~ ~O Cephalopod male I Needham Sac : : : : : : : :\!!(.z:>~ , Argonautoidea male I~ I Conventional boundaries coelomic membrane - f?2{'){{~ Fig I I gonoducts gonad oviductal gland ~~j I -• General schemes of reproductive system structure in cephalopods I nidamental glands spermatophoric gland hectocotylus site of sexual product accu mu lation I I 65 66 J Northw Atl Fish ScL, Vol 12, 1992 Development and Function of the Reproductive System Wells, 1977) Gonads are unpaired in cuttlefish and squid from the start (LeMaire 1972; Fioroni, 1978) The development of the reproductive system takes place in several phases as follows: Females Oogenesis is similar in different cephalopod groups (Arnold and Williams-Arnold, 1977) An oocyte develops in successive stages from a simple to a complex follicle followed by vitellogenesis which ends in follicle expulsion and ovulation Despite the similarity, the stages are evidently not identical The most important difference is the time of nucleoli decomposition and R-RNA penetration in oocyte cytoplasm observed in different species with different follicle condition In Lol/iguncula brevis, AI/oteuthis subulata, Loligo opalescens, Octopus tehuelcus and Dosidicus gigas this takes place during intercalation (COWden, 1968; Bottke, 1974; Knipe and Beeman, 1978; Pujals, 1986; Michel et al., 1986) Disappearance of nucleoli in II/ex argentinus precedes the formation of folds in the follicular epithelium (Shuldt, 1979) Examination of oocytes in different developmental stages by Laptikhovsky (AtlantNIRO, Kaliningrad, USSR, pers comm.) suggests different episodes of nucleoli appearance and disappearance Nucleoli are not distinguishable before simple follicle formation in Octopoteuthis sicula, Sepia bertheloti and Abraliopsis atlantica In Argonauta argo and Pteriqioteutnis gemmata, at the stage when the simple follicle nucleoli start decomposing, they acquire a characteristic blot shape as observed in IIlex argentinus (Shuldt, 1979) In Octopus vulgaris, nucleoli remain unaltered until complex follicle formation and probably, disappear just before vitellogenesis begins Juvenile - the gonad forms, the germinal epithelium differentiates and accessory glands form Physiological maturation - formation of mature sexual cells takes place in the gonad, i.e oogenesis or spermatogenesis Accessory glands grow and their parts form Physiological maturity - mature sexual cells are expelled from the gonad to the sexual coelom Functional maturation - mature sexual cells ripen for spawning In females, this involves formation of additional oocyte coverings and the process of transferring oocytes into the organs from which spawning will take place In males this involves formation of spermatophores which provide for the transfer of spermatozoa to the female without loss Functional maturity - the reproductive system is completely ready for spawning In the simplest case, which is spawning into the water without preliminary treatment by accessory gland secretions (Patella, primitive mussels), the organism is ready for spawning at physiological maturity In higher forms (higher Gastropoda, Cephalopoda) the mature sexual cells undergo a number of processes (formation of additional coverings and formation of spermatophores) before spawning occurs In monocyclic animals, which represents the majority of living cephalopods (Nesis, 1985), the reproductive system undergoes the first three phases only once, and the fourth and fifth phases either once for one-time-only spawners or repeatedly for species that spawn more than once The following description of the main processes which take place during reproductive system development in different groups of cephalopods is aimed at providing a basis for further subdivision into stages of maturity as well as a consideration of the evolution of reproductive strategies The processes which take place during maturation of the sexual cells (i.e juvenile phase and physiological matu ration) are treated separately from the processes of further development and treatment of these cells (i.e physiological maturity to functional maturity) Males Spermatogenesis also varies in different cephalopods In Loligo opalescens primary spermatocytes have not been observed in maturing nor mature individuals (Grieb and Beeman, 1978) In mature IIlex argentinus not only primary spermatocytes but gonial cells also are found in the testis (Shuldt, 1979) In octopus, protoplasmic growth of spermatozoa in the gonad as well as gonoduct development take place independent of optic gland activity (Buckley, 1976) In castrated juvenile octopus, spermducts and spermatophoric glands develop normally (Taki, 1945; Wells and Wells, 1977) This suggests that during the juvenile phase and through physiological maturation, the gonad and accessory glands function asynchronously At physiological maturity these two organs function synchronously Preliminary activity in accessory glands takes place shortly before the mature sexual cells are expelled, i.e formation of preliminary spermatophores takes place in the spermatophoric gland (Laptikhovsky and Nigmatullin, 1987) Juvenile phase and physiological maturation Physiological maturity, functional maturation and maturity Initially the embryonic gonad in octopus is paired but it becomes fused in young animals (Wells and Females The simplest type of reproductive system is found in octopus In primitive octopus of the sub- ARKHIPKIN: Reproductive System Structure, Development and Function in Cephalopods order Cirrata, ripe oocytes not accumulate in the coelom Rather, immediately after ovulation they are released one by one into the oviducts where they are covered with a thick shell formed by the secretion of the oviductal glands (Aldred et al., 1983; Boletzky, 1979) Short-term accumulation of oocytes in the coelom, and usually a single spawning, occur in octopus of the suborder Incirrata Octopus zonatus, in which repeated spawning has been observed (Rodaniche, 1984), is an exception In cuttlefish, mature oocytes accumulate mostly in the coelom but partially in the proximal ends of the oviducts which form a wide, concaved funnel Mature oocytes accumulate in the oviducts of squid in preparation for spawning Spawning occurs only once in Todarodes pacificus (Hamabe, 1962) but the process of oocyte accumulation in the oviducts is repeated in multiple spawners such as Thysanoteuthis rhombus (Arkhipkin et al., 1983), Berryteuthis magister (Reznik, 1983) and Stenoteuthis oualaniensis (Harman et al., 1989) It is important to clarify the homology of accessory glands in cephalopods Gastropod accessory glands are different in origin, and form egg coverings at spawning A mucous secretion is formed by pallial, pedal and hypobranchial glands in different species of this class In mollusks which lay their eggs in rigid capsules, capsule glands and albumin glands are present in a complex of pallial glands These differ in their origin and function (Chukchin, 1984) Oviductal glands in octopus secrete an adhesive cement, while those of cuttlefish and squid secrete a light mucous which forms the third egg covering Nidamental glands in squid and cuttlefish also differ both in form and secretion In cuttlefish the secretion is a fourth covering forming thick egg capsules, but in squid the nidamental glands secrete a mucous mass at spawning Octopus and cuttlefish usually lay eggs one by one on the substrate When several are laid at the same time, a cluster of individual eggs is formed The eggs are sheltered and protected by the female in octopus but not in cuttlefish In squid, with the exception of Enoploteuthinae, (Young and Harman, 1985), eggs form a complex structure At spawning, eggs are immersed in a mucous secretion of nidamental glands which forms the fourth covering (Hamabe, 1962) The mucous is inedible and provides protection for embryos to develop within the mass In squid, each spawning tends to be specific in terms of size and number of eggs (Hamabe, 1962; Sanzo, 1929; Sabirov et al., 1987) Thus accumulation of ripe eggs must be synchronized with secreting 67 accessory glands for successful formation of the egg mass at spawning In squid, oocytes at different stages of development are found within the gonad at the same time If ripe eggs are accumulated in the coelom', as in some octopus and cuttlefish, all the oocytes in the gonad would be laid at the same time Possibly, benthopelagic or nektobenthic ancestors of squid spawned this way but there is probably survival advantage for monocyclic animals with a short life span inhabiting various environments in laying portions of their total fecundity periodically Asynchrony in gonad development and accumulation of portions of mature oocytes in the oviducts rather than in the coelom may be an adaptation by squid that enhances survival of young Males As spermatozoa mature and are released from the testis they pass directly to the spermaduct which is surrounded by a complex of accessory glands The first glands inactivate the spermatozoa and others cover the sperm mass with different secretions to form the spermatophore (Drew, 1919) Spermatophores usually accumulate in the Needham sac Each spermatophore is therefore analogous to a single egg laying of a female squid Usually only a portion of the spermatophores from the Needham sac is transferred to any female Males of the most primitive recent cephalopods (octopus of the suborder Cirrata) produce sperm packets rather than spermatophores In each of these packets spermatozoa are positioned with their tails towards the centre and heads towards the periphery (Aldred et al., 1983) In octopus of the Arqonautoidea superfamily (Fig 1) only one spermatophore is formed in the spermducts This spermatophore "bursts" in the Needham sac and its contents are transferred to the seminal reservoir on a specialized arm called the hectocotylus The hectocotylus detaches during copulation and is inserted into the female mantle cavity (Nesis, 1982) In primitive mussels (Monoplacophora and others) the male sexual system is organized and functions similarly to that of female octopus, i.e sperm accumulate in sexual coelom and are released into the spermduct at spawning In primitive prosobranch mollusks (Littorina) the male sexual system functions similarly to that of female squid, i.e sperm accululate in the enlarged part of the spermduct In higher prosobranchs (Ptenoglossa), spermatozoa are formed into special structures called spermatozeugmae which are able to move actively (Chukchin, 1984) In some higher gastropods (pulmonate mollusks - Stylommastophora), spermatophore formation takes place in the sexual viae and accumulate in the Needham sac which is similar to what occurs in some cephalopod males In higher gastropods, sperm is transferred to the female cloaca by a special copulatory organ (penis), 68 J Northw Atl Fish ScL, Vol 12, 1992 which is either a body wall protrusion or a modified tentacle In cephalopods, the distal part of the Needham sac has slightly muscular walls and forms what is termed a "penis" which serves not for internal fertilization but for sperm transfer This transfer is either directly to a female (for example, in squid (Onyehoteuthis sp.)) with a long penis or in most cases to the hectocotylized part of a ventral arm (in squid (Ommastrephes sp and others)) with a short penis Types of Reproductive Strategy and Evolution Differences in reproductive system structure and function (particularly in females) suggest how living cephalopod groups may have evolved to occupy various ecological niches in the ocean All living cephalopods appeared in the Early Paleocene which is relatively recent in geological time Division of Orders took place in the Upper Triassic-Early Jurassic and the main orders developed in the Neocene Apparently, main types of reproductive system structure were already formed by the Mesozoic era in all three orders and remained order specific in spite of the fact that many species with different life styles evolved within each order in the Neocene (Nesis, 1985) Cephalopods with similar life styles but belonging to different orders did not evolve similar reproductive systems during a short geological time period For example, species of living octopus, cuttlefish and squid inhabit oceanic waters pelagically but have different types of reproductive systems However, other living forms from different orders evolved similar benthopelagic life styles during a long geological time period For example, nautilus and finned octopus lay eggs one by one on the bottom with a thick skin-like shell protecting the embryo from unfavourable environmental conditions and predators Octopus As octopus of the suborder Incirrata developed the benthic mode of life, their reproductive strategy changed considerably from their ancestors (Fig 2) In all species of Incirrata, eggs accumulate in the coelom in small (deep-water Benthoctopus, Benthe/edone) or large quantities (some of Octopus, E/edone) and are then released in a single spawning Eggs are attached individually to shelters by means of oviducal gland secretions Eggs are usually protected by females (Boletzky, 1981) As a rule, females die after eggs hatch In small-egged species there is indirect development with a pelagic larva while in large-egged species there is direct development to bottom-dwelling juveniles Since most octopus are large-egged, kselection dominates with r-selection appearing only in small-egged species (Boletzky, 1981) As octopus (especially holopelagic species) developed a pelagic mode of life, the main characteristic of their benthic ancestors, protection of eggs by the females, was retained as they entered the midwater Females of the family Alloposidae possibly lay eggs at the bottom in spite of their own planktonic mode of life (Nesis, 1982) Females of epipelagic species Tremoetopus vio/aeeus, as well as those of midwater species of Bolitanidae and Amphitretidae families, bear eggs in their arms, similar to bottom dwelling Hapa/oeh/aena maeu/osa Argonauta, to protect eggs borne in arms, developed a shell which is not homologous to that of nautilus (Boletzky, 1981) Finally, development of eggs in the oviducts (ovoviviparity) is observed in epipelagic Oeythoe and midwater Vitre/edonella Thus, in all these octopus where eggs are protected up to the moment larvae are hatched and at which time they enter the pelagic layers, k-selection dominates Cuttlefish Reproductive strategies of cuttlefish are different from those of octopus (Fig 2) They are mainly nektobenthic animals which also accumulate eggs in the coelom similar to octopus, however, before spawning the eggs are covered with oviducal gland secretions and also with a thick capsule secreted by the nidamental glands Eggs are laid one by one or in clusters in different kinds of shelters or on hard substrates and are usuallylett unprotected (Choe, 1966) Females of some species cover eggs with ink or "roll" them in sand (Boletzky, 1983) Since eggs of cuttlefish are heavier than water (due to the thick, hard shell) no species of this order has become holopelagic Within the order, a transition to the benthic mode of life has occurred in Rossinae, Sepiolinae, Sepiadaridae Both micronektonic Heteroteuthis (Boletzky, 1978) and planktonic Spiru/a are "forced" to lay eggs on the bottom and their distribution is restricted to continental shelf waters Among sepiids there are both large-egged species with bottom-dwelling juveniles (Sepiidae, Sepiadaridae, Sepiolidae) and small-egged species with pelagic larvae (Idiosepidae, Heteroteuthis) In cuttlefish, as in octopus, k-selection dominates with r-selection only in small-egged species Squid Squid exhibit a third kind of reproductive strategy (Fig 2) Their nidamental glands secrete a neutrally buoyant mucous mass in which eggs are suspended (O'Dor and Balch, 1985) This has enabled squid to develop the most characteristic lifestyle among cephalopods, especially habitation of pelagic waters of the open ocean Fecundity is low in squid inhabiting shelf areas where the bottom provides a stable substrate for egg laying In reef-living Sepioteuthis, only to eggs are laid in a mucous string which is hidden by the female (LaRoe, 1971) The fecundity of shelf-living squid is usually several hundred to several thousand eggs (Lo/igo sp.) High fecundity is found in squid which ARKHIPKIN: Reproductive System Structure, Development and Function in Cephalopods 69 Nautilida, Octopoda Planktonic ~t:;==:JCSfr Holopelagic Vitrelenellidae Bolitaenidae Amphitretidae OCythOB Argonauta Tremoctopus -~(;=:::::,-Hemipelagic ,U